A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici

Abstract Background The gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes...

Full description

Bibliographic Details
Main Authors: Thomas Badet, Ursula Oggenfuss, Leen Abraham, Bruce A. McDonald, Daniel Croll
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Biology
Online Access:https://doi.org/10.1186/s12915-020-0744-3
_version_ 1818610159651389440
author Thomas Badet
Ursula Oggenfuss
Leen Abraham
Bruce A. McDonald
Daniel Croll
author_facet Thomas Badet
Ursula Oggenfuss
Leen Abraham
Bruce A. McDonald
Daniel Croll
author_sort Thomas Badet
collection DOAJ
description Abstract Background The gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. Results Here, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only ~ 60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable element content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species. Conclusions Taken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.
first_indexed 2024-12-16T15:10:00Z
format Article
id doaj.art-8aadf1d8163b48f3928cce1726b21b9c
institution Directory Open Access Journal
issn 1741-7007
language English
last_indexed 2024-12-16T15:10:00Z
publishDate 2020-02-01
publisher BMC
record_format Article
series BMC Biology
spelling doaj.art-8aadf1d8163b48f3928cce1726b21b9c2022-12-21T22:27:00ZengBMCBMC Biology1741-70072020-02-0118111810.1186/s12915-020-0744-3A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria triticiThomas Badet0Ursula Oggenfuss1Leen Abraham2Bruce A. McDonald3Daniel Croll4Laboratory of Evolutionary Genetics, Institute of Biology, University of NeuchâtelLaboratory of Evolutionary Genetics, Institute of Biology, University of NeuchâtelLaboratory of Evolutionary Genetics, Institute of Biology, University of NeuchâtelPlant Pathology, Institute of Integrative Biology, ETH ZürichLaboratory of Evolutionary Genetics, Institute of Biology, University of NeuchâtelAbstract Background The gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. Results Here, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only ~ 60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable element content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species. Conclusions Taken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.https://doi.org/10.1186/s12915-020-0744-3
spellingShingle Thomas Badet
Ursula Oggenfuss
Leen Abraham
Bruce A. McDonald
Daniel Croll
A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
BMC Biology
title A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
title_full A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
title_fullStr A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
title_full_unstemmed A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
title_short A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
title_sort 19 isolate reference quality global pangenome for the fungal wheat pathogen zymoseptoria tritici
url https://doi.org/10.1186/s12915-020-0744-3
work_keys_str_mv AT thomasbadet a19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT ursulaoggenfuss a19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT leenabraham a19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT bruceamcdonald a19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT danielcroll a19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT thomasbadet 19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT ursulaoggenfuss 19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT leenabraham 19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT bruceamcdonald 19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici
AT danielcroll 19isolatereferencequalityglobalpangenomeforthefungalwheatpathogenzymoseptoriatritici